Later, he worked as a researcher at the University of Freiburg. From 1966 to 1995, he worked at the Institute for modern history in Ljubljana. Until his retirement in 2013 he worked as professor at the Faculty of Social Sciences[1] of the University of Ljubljana.

Prunk has been actively involved in politics. As an early admirer of Jože Pučnik, Prunk joined the Democratic Opposition of Slovenia after the democratization of Slovenia. He was an active member of the Slovenian Democratic Party (known as Slovenian Social Democratic Party between 1989 and 2003). Between 1992 and 1993, Prunk served as Minister for Slovenes outside Slovenia and National Minorities in Slovenia in the first coalition cabinet[2] of Janez Drnovšek.

After 1994, Prunk withdrew from politics for over a decade. Before the parliamentary elections of 2004, he campaigned for the Slovenian Democratic Party. In 2005, he was appointed by the Foreign Minister Dimitrij Rupel, as president of the Slovene-Croatian Historical Commission,[3] formed by the Government of the two countries, to shed light on the history of the relations between them.[4] Between 2004 and 2008, he served as chairman of the Slovenian Democratic Party's internal Committee for Education Policies. He resigned in 2008 because of disagreements over the Government's policy favoring private universities. After the split with the party, he became very critical of the then Prime Minister Janez Janša, whom he accused of being a "liberal with an authoritative touch, who aspires at becoming a Slovenian Piłsudski".[5]

After the parliamentary elections of 2008, Prunk explained his disappointment with the Slovenian Democratic Party as a consequence of its neo-liberal turn. In Prunk's opinion, the party turned its back to the ideals of welfare state held by its founding father Jože Pučnik.[6] Prunk also criticised the charismatic type of leadership of the party's president Janez Janša, stating that the party would most probably collapse if Janša resigned.[6]

Janko Prunk has written over 400 specialized articles and books, since 1966. His book, A brief history of Slovenia: Historical background of the Republic of Slovenia,[7] is one of the most comprehensive works on modern Slovenian history.[8][9]